Richard D. Bardgett

HERBIVORE‐MEDIATED LINKAGES BETWEEN ABOVEGROUND AND BELOWGROUND COMMUNITIES

Understanding how terrestrial ecosystems function requires a combined aboveground–belowground approach, because of the importance of feedbacks that occur between herbivores, producers, and the decomposer subsystem. In this paper, we identify several mechanisms by which herbivores can indirectly affect decomposer organisms and soil processes through altering the quantity and quality of resources entering the soil. We show that these mechanisms are broadly similar in nature for both foliar and root herbivory, regardless of whether they operate in the short term as a result of physiological responses of individual plants to herbivore attack or long-term following alteration of plant community structure by herbivores and subsequent changes in the quality of litter inputs to soil. We propose that a variety of possible mechanisms is responsible for the idiosyncratic nature of herbivore effects on soil biota and ecosystem function; positive, negative, or neutral effects of herbivory are possible depending upon the balance of these different mechanisms. However, we predict that positive effects of herbivory on soil biota and soil processes are most common in ecosystems of high soil fertility and high consumption rates, whereas negative effects are most common in unproductive ecosystems with low consumption rates. The significance of multiple-species herbivore communities is also emphasized, and we propose that if resource use complementarity among herbivore species or functional groups leads to greater total consumption of phytomass, and thus greater net herbivory, then both positive and negative consequences of increasing herbivore diversity for belowground properties and processes are theoretically possible. Research priorities are highlighted and include a need for comparative studies of herbivore impacts on above- and belowground processes across ecosystems of varying productivity, as well as a need for experimental testing of the influence of antiherbivore defense compounds on complex multitrophic interactions in the rhizosphere and the significance of multiple herbivore species communities on these plant–soil interactions.

Plant functional traits and soil carbon sequestration in contrasting biomes

Plant functional traits control a variety of terrestrial ecosystem processes, including soil carbon storage which is a key component of the global carbon cycle. Plant traits regulate net soil carbon storage by controlling carbon assimilation, its transfer and storage in belowground biomass, and its release from soil through respiration, fire and leaching. However, our mechanistic understanding of these processes is incomplete. Here, we present a mechanistic framework, based on the plant traits that drive soil carbon inputs and outputs, for understanding how alteration of vegetation composition will affect soil carbon sequestration under global changes. First, we show direct and indirect plant trait effects on soil carbon input and output through autotrophs and heterotrophs, and through modification of abiotic conditions, which need to be considered to determine the local carbon sequestration potential. Second, we explore how the composition of key plant traits and soil biota related to carbon input, release and storage prevail in different biomes across the globe, and address the biome-specific mechanisms by which plant trait composition may impact on soil carbon sequestration. We propose that a trait-based approach will help to develop strategies to preserve and promote carbon sequestration.

Diversity meets decomposition

Over 100 gigatons of terrestrial plant biomass are produced globally each year. Ninety percent of this biomass escapes herbivory and enters the dead organic matter pool, thus supporting complex detritus-based food webs that determine the critical balance between carbon mineralization and sequestration. How will changes in biodiversity affect this vital component of ecosystem functioning? Based on our analysis of concepts and experiments of leaf decomposition in forest floors and streams, we suggest that changes in species diversity within and across trophic levels can significantly alter decomposition. This happens through various mechanisms that are broadly similar in forest floors and streams. Differences in diversity effects between these systems relate to divergent habitat conditions and evolutionary trajectories of aquatic and terrestrial decomposers.

Linking above-ground and below-ground interactions: How plant responses to foliar herbivory influence soil organisms

Abstract Studies of the effects of above-ground herbivory on soil organisms and decomposer food webs, as well as the processes that they regulate, have largely concentrated on the effects of non-living inputs into the soil, such as dung, urine, body parts and litter. However, there is an increasing body of information which points to the importance of plant physiological responses to herbivory in regulating soil organisms and therefore, implicitly, key soil processes such as decomposition and nutrient mineralisation. In this review we identify the mechanisms by which foliar herbivory may indirectly affect the soil biota and associated below-ground processes through affecting plants, so as to better understand the nature of interactions which exist between above-ground and below-ground biota. We consider two broad pathways by which above-ground foliar herbivory may affect soil biotic communities. The first of these occurs through herbivore effects on patterns of root exudation and carbon allocation. These effects manifest themselves either as short-term changes in plant C allocation and root exudation or as long-term changes in root biomass and morphology. Evidence suggests that these mechanisms positively influence the size and activity of the soil biotic community and may alter the supply of nutrients in the rhizosphere for plant uptake and regrowth. The second of these involves herbivores influencing soil organisms through altering the quality of input of plant litter. Possible mechanisms by which this occurs are through herbivory enhancing nitrogen contents of root litter, through herbivory affecting production of secondary metabolites and concentrations of nutrients in foliage and thus in leaf litter and through selective foliar feeding causing shifts in plant community structure and thus the nature of litter input to the soil. While the effects of herbivory on soil organisms via plant responses may be extremely important, the directions of these effects are often unpredictable because several mechanisms are often involved and because of the inherently complex nature of soil food-web interactions; this creates obvious difficulties in developing general principles about how herbivory affects soil food-webs. Finally, it is apparent that very little is understood on how responses of soil organisms to herbivory affect those ecosystem-level processes regulated by the soil food-web (e.g. decomposition, nutrient mineralisation) and that such information is essential in developing a balanced understanding about how herbivory affects ecosystem function.

Plant-soil feedbacks: The past, the present and future challenges

Summary Plant–soil feedbacks is becoming an important concept for explaining vegetation dynamics, the invasiveness of introduced exotic species in new habitats and how terrestrial ecosystems respond to global land use and climate change. Using a new conceptual model, we show how critical alterations in plant–soil feedback interactions can change the assemblage of plant communities. We highlight recent advances, define terms and identify future challenges in this area of research and discuss how variations in strengths and directions of plant–soil feedbacks can explain succession, invasion, response to climate warming and diversity-productivity relationships. While there has been a rapid increase in understanding the biological, chemical and physical mechanisms and their interdependencies underlying plant–soil feedback interactions, further progress is to be expected from applying new experimental techniques and technologies, linking empirical studies to modelling and field-based studies that can include plant–soil feedback interactions on longer time scales that also include long-term processes such as litter decomposition and mineralization. Significant progress has also been made in analysing consequences of plant–soil feedbacks for biodiversity-functioning relationships, plant fitness and selection. To further integrate plant–soil feedbacks into ecological theory, it will be important to determine where and how observed patterns may be generalized, and how they may influence evolution. Synthesis. Gaining a greater understanding of plant–soil feedbacks and underlying mechanisms is improving our ability to predict consequences of these interactions for plant community composition and productivity under a variety of conditions. Future research will enable better prediction and mitigation of the consequences of human-induced global changes, improve efforts of restoration and conservation and promote sustainable provision of ecosystem services in a rapidly changing world.

PLANT REMOVALS IN PERENNIAL GRASSLAND: VEGETATION DYNAMICS, DECOMPOSERS, SOIL BIODIVERSITY, AND ECOSYSTEM PROPERTIES

The consequences of permanent loss of species or species groups from plant communities are poorly understood, although there is increasing evidence that individual species effects are important in modifying ecosystem properties. We conducted a field experiment in a New Zealand perennial grassland ecosystem, creating artificial vegetation gaps and imposing manipulation treatments on the reestablishing vegetation. Treatments consisted of continual removal of different subsets or “functional groups” of the flora. We monitored vegetation and soil biotic and chemical properties over a 3-yr period. Plant competitive effects were clear: removal of the C3 grass Lolium perenne L. enhanced vegetative cover, biomass, and species richness of both the C4 grass and dicotyledonous weed functional groups and had either positive or negative effects on the legume Trifolium repens L., depending on season. Treatments significantly affected total plant cover and biomass; in particular, C4 grass removal reduced total plant biomass in summer, because no other species had appropriate phenology. Removal of C3 grasses reduced total root biomass and drastically enhanced overall shoot-to-root biomass ratios. Aboveground net primary productivity (NPP) was not strongly affected by any treatment, indicating strong compensatory effects between different functional components of the flora. Removing all plants often negatively affected three further trophic levels of the decomposer functional food web: microflora, microbe-feeding nematodes, and predaceous nematodes. However, as long as plants were present, we did not find strong effects of removal treatments, NPP, or plant biomass on these trophic groupings, which instead were most closely related to spatial variation in soil chemical properties across all trophic levels, soil N in particular. Larger decomposer organisms, i.e., Collembola and earthworms, were unresponsive to any factor other than removal of all plants, which reduced their populations. We also considered five functional components of the soil biota at finer taxonomic levels: three decomposer components (microflora, microbe-feeding nematodes, predaceous nematodes) and two herbivore groups (nematodes and arthropods). Taxa within these five groups responded to removal treatments, indicating that plant community composition has multitrophic effects at higher levels of taxonomic resolution. The principal ordination axes summarizing community-level data for different trophic groups in the soil food web were related to each other in several instances, but the plant ordination axes were only significantly related to those of the soil microfloral community. There were time lag effects, with ordination axes of soil-associated herbivorous arthropods and microbial-feeding nematodes being related to ordination axes representing plant community structure at earlier measurement dates. Taxonomic diversity of some soil organism groups was linked to plant removals or to plant diversity. For herbivorous arthropods, removal of C4 grasses enhanced diversity; there were negative correlations between plant and arthropod diversity, presumably because of negative influences of C4 species in the most diverse treatments. There was evidence of lag relationships between diversity of plants and that of the three decomposer groups, indicating multitrophic effects of altering plant diversity. Relatively small effects of plant removal on the decomposer food web were also apparent in soil processes regulated by this food web. Decomposition rates of substrates added to soils showed no relationship with treatment, and rates of CO2 evolution from the soil were only adversely affected when all plants were removed. Few plant functional-group effects on soil nutrient dynamics were identified. Although some treatments affected temporal variability (and thus stability) of soil biotic properties (particularly CO2 release) throughout the experiment, there was no evidence of destabilizing effects of plant removals. Our data provide evidence that permanent exclusion of plant species from the species pool can have important consequences for overall vegetation composition in addition to the direct effects of vegetation removal, and various potential effects on both the above- and belowground subsystems. The nature of many of these effects is driven by which plant species are lost from the system, which depends on the various attributes or traits of these species.

Belowground biodiversity and ecosystem functioning

Evidence is mounting that the immense diversity of microorganisms and animals that live belowground contributes significantly to shaping aboveground biodiversity and the functioning of terrestrial ecosystems. Our understanding of how this belowground biodiversity is distributed, and how it regulates the structure and functioning of terrestrial ecosystems, is rapidly growing. Evidence also points to soil biodiversity as having a key role in determining the ecological and evolutionary responses of terrestrial ecosystems to current and future environmental change. Here we review recent progress and propose avenues for further research in this field.

Microbial contributions to climate change through carbon cycle feedbacks

There is considerable interest in understanding the biological mechanisms that regulate carbon exchanges between the land and atmosphere, and how these exchanges respond to climate change. An understanding of soil microbial ecology is central to our ability to assess terrestrial carbon cycle–climate feedbacks, but the complexity of the soil microbial community and the many ways that it can be affected by climate and other global changes hampers our ability to draw firm conclusions on this topic. In this paper, we argue that to understand the potential negative and positive contributions of soil microbes to land–atmosphere carbon exchange and global warming requires explicit consideration of both direct and indirect impacts of climate change on microorganisms. Moreover, we argue that this requires consideration of complex interactions and feedbacks that occur between microbes, plants and their physical environment in the context of climate change, and the influence of other global changes which have the capacity to amplify climate-driven effects on soil microbes. Overall, we emphasize the urgent need for greater understanding of how soil microbial ecology contributes to land–atmosphere carbon exchange in the context of climate change, and identify some challenges for the future. In particular, we highlight the need for a multifactor experimental approach to understand how soil microbes and their activities respond to climate change and consequences for carbon cycle feedbacks.

Microorganisms and climate change: Terrestrial feedbacks and mitigation options

Microbial processes have a central role in the global fluxes of the key biogenic greenhouse gases (carbon dioxide, methane and nitrous oxide) and are likely to respond rapidly to climate change. Whether changes in microbial processes lead to a net positive or negative feedback for greenhouse gas emissions is unclear. To improve the prediction of climate models, it is important to understand the mechanisms by which microorganisms regulate terrestrial greenhouse gas flux. This involves consideration of the complex interactions that occur between microorganisms and other biotic and abiotic factors. The potential to mitigate climate change by reducing greenhouse gas emissions through managing terrestrial microbial processes is a tantalizing prospect for the future.

Towards an assessment of multiple ecosystem processes and services via functional traits

Managing ecosystems to ensure the provision of multiple ecosystem services is a key challenge for applied ecology. Functional traits are receiving increasing attention as the main ecological attributes by which different organisms and biological communities influence ecosystem services through their effects on underlying ecosystem processes. Here we synthesize concepts and empirical evidence on linkages between functional traits and ecosystem services across different trophic levels. Most of the 247 studies reviewed considered plants and soil invertebrates, but quantitative trait–service associations have been documented for a range of organisms and ecosystems, illustrating the wide applicability of the trait approach. Within each trophic level, specific processes are affected by a combination of traits while particular key traits are simultaneously involved in the control of multiple processes. These multiple associations between traits and ecosystem processes can help to identify predictable trait–service clusters that depend on several trophic levels, such as clusters of traits of plants and soil organisms that underlie nutrient cycling, herbivory, and fodder and fibre production. We propose that the assessment of trait–service clusters will represent a crucial step in ecosystem service monitoring and in balancing the delivery of multiple, and sometimes conflicting, services in ecosystem management.